Context Matters: Contrasting Ladybird Beetle Responses to Urban Environments across Two US Regions - MDPI
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sustainability
Article
Context Matters: Contrasting Ladybird Beetle
Responses to Urban Environments across Two
US Regions
Monika Egerer 1, * ID
, Kevin Li 2 and Theresa Wei Ying Ong 3,4 ID
1 Environmental Studies Department, University of California, Santa Cruz, Santa Cruz, CA 95064, USA
2 Department of Plant Sciences, University of Göttingen, Göttingen NI 37077, Germany;
kevin.li@uni-goettingen.de
3 Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA;
wyong@princeton.edu
4 Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08540, USA
* Correspondence: megerer@ucsc.edu; Tel.: +1-734-775-8950
Received: 8 April 2018; Accepted: 30 May 2018; Published: 1 June 2018
Abstract: Urban agroecosystems offer an opportunity to investigate the diversity and distribution
of organisms that are conserved in city landscapes. This information is not only important for
conservation efforts, but also has important implications for sustainable agricultural practices.
Associated biodiversity can provide ecosystem services like pollination and pest control, but because
organisms may respond differently to the unique environmental filters of specific urban landscapes,
it is valuable to compare regions that have different abiotic conditions and urbanization histories.
In this study, we compared the abundance and diversity of ladybird beetles within urban gardens in
California and Michigan, USA. We asked what species are shared, and what species are unique
to urban regions. Moreover, we asked how beetle diversity is influenced by the amount and
rate of urbanization surrounding sampled urban gardens. We found that the abundance and
diversity of beetles, particularly of unique species, respond in opposite directions to urbanization:
ladybirds increased with urbanization in California, but decreased with urbanization in Michigan.
We propose that in California water availability in gardens and the urbanization history of the
landscape could explain the divergent pattern. Thus, urban context is likely a key contributor to
biodiversity within habitats and an important consideration for sustainable agricultural practices in
urban agroecosystems.
Keywords: urban gardens; biological control; impervious surface; urbanization rate; Michigan; California
1. Introduction
Urbanization is changing biodiversity patterns and population distributions in cities across
the world [1,2]. Urban environments are characterized by changes in abiotic [3] as well as biotic
conditions [4]. For example, greater amounts of impervious surface in cities causes urban heat island
effects, which increases the temperatures of cities [5] and within urban green spaces [6]. Light pollution
from buildings and car traffic extends the duration and intensity of light availability, affecting the
circadian rhythms of biotic elements [7]. Irrigation of lawns, parks and gardens adds water resources
and maintains the presence of vegetation for organisms to exploit [8,9]. Moreover, the abundance and
distribution of species and resources (habitat/food/shelter) in urban areas are often supplemented or
altered across time and space [1,10].
Changes in environmental conditions and resource availability have different effects on different
taxa and species [1,11]. Some species are able to persist and thrive in altered urban environments,
Sustainability 2018, 10, 1829; doi:10.3390/su10061829 www.mdpi.com/journal/sustainabilitySustainability 2018, 10, 1829 2 of 17
while environmental filters and competition can cause other species to decline [12]. The species that
thrive, what some consider “urban exploiters”, are often habitat generalists that are able to live, exploit
resources and reproduce in diverse, resource poor environmental conditions [2]. On the other hand,
specialist species with particular habitat (food, shelter) requirements may be more sensitive to—and
decline with—increasing urbanization because cities do not have the vegetation or resources to support
these species [13]. The negative effect(s) of urbanization on species life history and functional traits
may lead to biotic homogenization and declines in species richness within urban habitats [14].
The rate at which urbanization occurs (i.e., the speed at which land is converted to impervious
surface) could further affect the diversity and distribution of species abundance and richness within
urban habitats, and their ability to adapt to certain urban conditions. The percent impervious surface
is forecasted to increase by 1.5 million km2 by 2030 [15,16]. Moreover, because cities have distinct
development histories, socio-cultural and demographic trends [17], it is important to understand
whether and how biodiversity will respond to increasing urbanization (and associated qualitative
and quantitative aspects) across multiple urban environmental contexts [16,18]. Elucidating whether
certain organisms respond differently or not between unique regions can inform conservation agendas
and urban sustainability broadly for various cities across the world [1,19].
Urban agroecosystems such as community and home gardens are high-quality habitats that
conserve considerable amounts of biodiversity in cities [20]. These systems are heavily managed by
people predominantly for the purpose of cultivating fresh vegetables, fruits, flowers and herbs for
self-consumption [21–23]. Because urban agroecosystems are usually vegetated and irrigated [24],
they provide food and shelter for many arthropods. Certain arthropod groups, for example pollinators
and natural enemies, are in turn important for providing ecosystem services like crop pollination and
pest control. Previous studies have shown that these arthropod groups are less abundant in gardens
where surrounding levels of urbanization are high [25,26]. However, groups respond differentially to
urbanization and at different spatial scales [27,28]. Some arthropod groups and species in urban
environments including urban agroecosystems may actually increase with urbanization [29,30].
For example, insect pollinator species diversity is greater in some urban regions compared to
surrounding suburban and agricultural areas [30–32]. Currently, it is unclear whether these patterns are
regional phenomena or if these trends are generalizable to other urban regional contexts. We argue that
this question warrants further investigation, requiring research that draws comparisons of arthropod
biodiversity across spatially distinct regions. Yet studies in urban agroecosystems that compare and
synthesize findings across regions with different environmental conditions are rare [33].
Here, we combine data on ladybird beetle abundance and species richness collected from
comparable urban agroecosystems in two distinct geographical regions to test whether the response
of ladybird beetles to urbanization differs by the environmental context and urbanization history.
Ladybird beetles are charismatic arthropods in agroecosystems that provide key natural pest
control services, particularly of herbivorous aphids, mites and scale insects [34–36]. Because urban
agroecosystems are situated among dense human populations, they tend towards organic,
environmentally friendly, and human-health-conscious forms of management [37]. Thus, natural
pest control is particularly important for these agroecosystems. In this study, we asked: (1) Does the
relationship between urbanization (percent impervious surface, rate of development) and predator
(ladybird beetle) systems in urban agroecosystems change with environmental context (region)?
(2) Which species are shared by, and which are unique to urban agroecosystems of different regions?
(3) Do shared species respond differently to urbanization measures in the region than unique species?
2. Methods
2.1. Study Regions
We worked in two regions in the USA—California and Michigan—to collect ladybird beetle data
in urban community gardens in these regions (Figure 1). In California, we collected ladybird beetleSustainability 2018, 10, 1829 3 of 17
data from 18 urban gardens in the California central coast in Santa Clara, Santa Cruz, and Monterey
counties, which have estimated population densities of 274, 232, and 50 people/sq. km, respectively
(2010–2014 U.S. census period) [38]. In Michigan, we collected ladybird beetle data from 13 urban
gardens in Washtenaw county, which has an estimated population density of 192 people/sq. km [38].
The gardens in both regions are surrounded by different amounts of impervious surface. Moreover,
the gardens differ in vegetation and groundcover composition and structure, but because they are
all community gardens, differences in composition and structure are assumed to be relatively similar
between regions. The gardens range in size from 444 to 15,525 m2 in California and from 54 to 8778 m2
in Michigan, and are separated by approximately >2 km in California and >0.5 km in Michigan. All of
the gardens have been cultivated for 1 to 47 years and do not use chemical pesticides and insecticides.
Figure 1. Study regions in Michigan (a) and in California (b) where community gardens (black circles)
were sampled. Increasing percent impervious surface (NLCD 2011) shown with increasing shaded color.
2.2. Ladybird Beetle Sampling
To assess ladybird beetle communities in the gardens, we used visual and trapping methods in
both regions. In California, we sampled for adult beetles with visual surveys and sticky traps within
20 m2 plots at the center of each of the 18 gardens six times during summer 2014 (17–20 June, 7–10 July,
27–30 July, 19–21 August, 8–10 September, 29 September–1 October). Within the 20 m2 , we visually
surveyed vegetation and ground cover for adult beetles in eight randomly placed 0.5 × 0.5 m sub-plots.
We collected all individuals observed and stored them in vials with ethyl alcohol. At four random
locations within the plots, we also placed a 300 × 500 yellow sticky trap card (BioQuip Products Inc.,
Compton, CA, USA) on a galvanized wire stake for 24 h. In Michigan, we sampled for adult beetles by
visually surveying five sentinel potted pea plants (Pisum sativum var. Dwarf grey) placed at each of the
13 gardens in Washtenaw County. Any ladybird beetle adults on plants were counted and identified to
species. In addition, we swept surrounding vegetation in gardens for adult ladybird beetles using 10
full sweeps of a 0.2 m diameter net. All Michigan gardens were surveyed twice a week from 14 MaySustainability 2018, 10, 1829 4 of 17
to 20 July 2012. Sampling effort was consistent in all sites in each region throughout the sampling
periods: in Michigan, the same two researchers conducted the sampling within the respective area
for 30 min; in California, the same researcher conducted the sampling within the respective area for
60 min. The slight differences in sampling methods and years sampled between regions introduces
some limitations discussed later in our conclusions.
We identified all ladybird beetles on traps and in vials to species using identification guides [39]
and online resources [40,41]. Total abundance for each site for each species, total species richness,
and total species diversity (Shannon’s Diversity Index H) was tabulated across the months. Species
diversity includes the relative distribution of species’ abundances and was calculated using the vegan
package in R [42]. For the analysis, we categorized species present in both California and Michigan as
“shared species”, and categorized species that were not both present in California and Michigan as
“unique species”.
2.3. Urban Landscape Analysis
To measure current levels of urbanization and to assess urbanization history, we summarized
(1) the mean percent impervious surface surrounding gardens, and (2) the rate at which percent
impervious surface has increased over time. For both regions (California, Michigan), we used the
package “raster” in R (v 3.4.1) [43,44] to calculate the mean percent impervious surface within buffers
of 10, 100, 500, 1000, 2000, 3000 m spatial scales surrounding each garden site based on land cover
data from the US Geological Survey’s National Land Cover Database (NLCD) 2011 Percent Developed
Imperviousness dataset [45]. Here, a high total percent impervious surface indicates higher degrees of
urbanization, and a low percent impervious surface indicates low degrees of urbanization. To calculate
the rate of percent impervious surface change over time (henceforth “urbanization rate”), we collected
this data at three time periods, as provided by the NLCD: 2001, 2006, 2011. Urbanization rate was
calculated as the slope of the regression across these three time periods.
2.4. Statistical Analysis
We ran species accumulation curves to test whether species richness had been sufficiently
sampled in both California and Michigan. The expected number of species in each geographic
region was calculated using a sample-based rarefaction method known as the Mao Tau estimator [46].
Both regions showed evidence that richness was sufficiently sampled, exhibiting saturation in their
species accumulation curves (Figure S1).
We first modeled abundance and richness for each region at multiple spatial scales to determine
the best scale at which ladybird beetles respond to urbanization. We built seven generalized linear
models (GLM) at 0, 10, 100, 500, 1000, 2000, 3000 m spatial scales assuming Poisson error distributions
for count data. The model with the lowest Akaike Information Criterion (AIC) was selected as the best
spatial scale for each region [47].
Urbanization rate was calculated by taking the slopes of linear regressions between time and
impervious surface (NLCD: 2001, 2006, 2011) for each garden at a scale of 500 m. This was the buffer
scale determined earlier to be significant for Michigan. California beetles best responded to impervious
cover at 100 m, but at this scale urbanization rate did not vary by garden. Thus, we only analyzed
effects of urbanization rate on ladybird beetle abundance, species richness and species diversity
at 500 m for both regions. We also ran Pearson’s r tests between values of urbanization rate and
impervious surface at both 100 and 500 m to test for correlations between explanatory variables.
Urbanization rate and impervious surface were not significantly correlated (Table S1).
To determine whether ladybird beetles significantly responded to percent impervious surface
or urbanization rates, we constructed GLMs at the spatial scale appropriate for the region and
predictor variable as described above. Abundance and species richness GLMs assumed Poisson
error distributions, and diversity GLMs assumed Gaussian. All GLMs were then fit by LaplaceSustainability 2018, 10, 1829 5 of 17
approximation and goodness of fit determined by Wald Z tests [47]. This is what we refer to in the text
as Poisson and linear regressions.
3. Results
We found 16 ladybird beetle species in California and eight species in Michigan over the sampling
periods across the regions (Table 1). Species diversity index values were higher in California (ranging
from 1.3 to 2.5 for all species) than in Michigan (ranging from 0 to 1.5). Only four species were shared
by California and Michigan, including: C. septempunctata, C. Sanguinea, H. axyridis and O. v-nigrum.
Thus, 12 species in California and four species in Michigan were unique to that region.
Total ladybird beetle species abundance, richness and diversity (shared and unique species) were
best explained by percent impervious surface at a 100 m spatial scale in California, but were best
explained at a 500 m spatial scale in Michigan (Table S2). Total ladybird beetle species abundance and
species diversity significantly increased with percent impervious surface in California, but significantly
declined with percent impervious surface in Michigan (Table 2; Figure 2). Total species richness also
generally increased in California and decreased in Michigan with percent impervious surface (Table 2).
The divergent trend between regions was similar for shared species: shared species abundance, richness
and diversity significantly increased in California with greater impervious surface, but were not
significant for response measures in Michigan (Table 2). Unique species abundance also significantly
increased with impervious cover in California, while unique species abundance significantly decreased
in Michigan (Table 2; Figure 2). Of note, impervious surface cover gradients were comparable between
California and Michigan.
In response to the rate of urbanization surrounding gardens, ladybird beetle abundance and
species diversity increased with faster urbanization rates in California (Table 2; Figure 3). Whereas,
in Michigan, it was not significant for all response measures (Table 2; Figure 3). Species diversity of
shared ladybird species significantly increased with faster urbanization rates for both regions (Table 2;
Figure 3). The abundance of unique species significantly increased in California and decreased in
Michigan with faster urbanization rates (Table 2; Figure 3).Sustainability 2018, 10, 1829 6 of 17
Table 1. Ladybird beetle species sampled in California and in Michigan. We present: the respective region the species was found in, their feeding habits, the ecological
role that they play in agroecosystems, their nativity in their respective region [39,48,49], and their current geographic distribution in the USA [39–41]. (CA = California;
MI = Michigan; NA = North America).
Ecological Function in
Species Region Observed Feeds on Origin Distribution in US
Agroecosystems
West coast, Northeast, few Midwest records (historically most
Adalia bipunctata CA aphids and mites predator/pest control native
of US and Canada)
Coccinella californica CA mostly aphids predator/pest control native West coast CA
Cycloneda polita CA mostly aphids predator/pest control native West coast US and British Columbia
Hippodamia convergens CA mostly aphids predator/pest control native Throughout US and western Canada
Hyperaspis quadrioculata CA aphids and scale insects predator/pest control native Central to south CA
Nephus binaevatus CA aphids and scale insects predator/pest control non-native Central to south CA
Psyllobora vigintimaculata CA fungus fungus and mildew control native Throughout US and Canada
Scymnus cervicalis CA mites and scale insects predator/pest and mite control native East US to south CA
Scymnus coniferarum CA mites and scale insects predator/pest and mite control native CA and scattered west NA records
Scymnus marginicollis CA mites and scale insects predator/pest and mite control native CA to British Columbia; scattered NA records
Scymnus nebulosus CA mites and scale insects predator/pest and mite control native South CA to Canada
Stethorus punctum CA mites and scale insects predator/pest and mite control native West coast US; Northeast, west to north Great Plains
Coleomegilla maculata MI mostly aphids predator/pest control native East NA to southwest US
Cryptolaemus montrouzieri MI mites and scale insects predator/pest and mite control non-native Throughout US
Hippodamia variegata MI mostly aphids predator/pest control native Northeastern to middle US and Canada
Propylea
MI mostly aphids predator/pest control non-native Throughout NA (native to the Palaearctic)
quatuordecimpunctata
Coccinella septempunctata MI, CA mostly aphids predator/pest control non-native Throughout NA (native to the Old World)
Cycloneda sanguinea MI, CA mostly aphids predator/pest control native West to south CA; NC and FL
Harmonia axyridis MI, CA mostly aphids predator/pest control non-native Throughout US and southern Canada, except northern Rockies
Olla v-nigrum MI, CA mostly aphids predator/pest control native Throughout US, except ME and Pacific NorthwestSustainability 2018, 10, 1829 7 of 17
Table 2. Results of regressions predicting ladybird beetle abundance (AB), richness (RI) and Shannon’s Diversity Index (SH) as a function of percent impervious
surface (IS) and urbanization rate (UR). Scale indicates the spatial scale in meters used to calculate predictor variables IS and UR. Coefficients and p values are derived
from Wald Z tests, which assess goodness of fit of generalized linear models to data assuming Poisson error distributions (AB, RI) or Gaussian error distribution (SH).
Dataset Region Scale Predicted Predictor Coefficient p-Value
All MI 500 AB IS −0.015 0.01
All CA 100 AB IS 0.019Sustainability 2018, 10, 1829 8 of 17
Sustainability 2018, 10, x FOR PEER REVIEW 8 of 17
Figure 2.Figure
Effect2.ofEffect of impervious surface on abundance, richness and diversity of ladybird beetles. Regressions of abundance, richness and diversity (Shannon Index)
impervious surface on abundance, richness and diversity of ladybird beetles. Regressions of abundance, richness and diversity (Shannon Index) of
of Michigan (black lines and points) and California ladybird beetles (red lines and points) as a function of % impervious surface at 500 m for MI and 100 m for CA.
Michigan (black lines and points) and California ladybird beetles (red lines and points) as a function of % impervious surface at 500 m for MI and 100 m for CA.
All species combined (a–c, top row), species that are shared by both CA and MI (d–f, middle row) and species unique to each region (g–i, bottom row). * indicate
All species combined (a–c, top row), species that are shared by both CA and MI (d–f, middle row) and species unique to each region (g–i, bottom row). * indicate
significant regressions (p < 0.05). In (b), Poisson regressions for MI and CA are partially significant (p < 0.10).
significant regressions (p < 0.05). In (b), Poisson regressions for MI and CA are partially significant (p < 0.10).Sustainability 2018, 10, 1829 9 of 17
Sustainability 2018, 10, x FOR PEER REVIEW 9 of 17
Figure 3.Figure
Effect3.ofEffect of urbanization rate on abundance, richness and diversity of ladybird beetles. Regressions of abundance, richness and diversity (Shannon Index) of
urbanization rate on abundance, richness and diversity of ladybird beetles. Regressions of abundance, richness and diversity (Shannon Index) of
Michigan (black lines and points) and California ladybird beetles (red lines and points) as a function of urbanization rate at 500 m. All species combined (a–c, top
Michigan (black lines and points) and California ladybird beetles (red lines and points) as a function of urbanization rate at 500 m. All species combined (a–c, top row),
row), species that are shared by both California and Michigan (d–f, middle row) and species unique to each region (g–i, bottom row). * indicate significant
species that are shared by both California and Michigan (d–f, middle row) and species unique to each region (g–i, bottom row). * indicate significant regressions
regressions (p < 0.05).
(p < 0.05).Sustainability 2018, 10, 1829 10 of 17
4. Discussion
The influence of urbanization on biodiversity can change with environmental (regional) context.
This comparative study between two urban regions in the US—California and Michigan—shows
that organisms respond differently to urbanization depending on region. Ladybird beetles have a
contrasting response to the intensity of urbanization as well as the rate at which urbanization occurs
in different regional contexts, and we found only one unidirectional relationship between species
diversity and urbanization rate between regions. The contrasting response is most apparent in the
abundance of all species and unique species. We hypothesize that the effect of urbanization on unique
species is driving this divergent pattern.
Our first question was whether the relationship between urbanization and ladybird beetles
in urban agroecosystems changes with environmental context. We found that urban gardens
are supporting more abundant and diverse ladybird beetle populations in more urban areas in
California, while in Michigan, ladybird beetles in urban gardens decline in abundance, species richness
and diversity with increasing amounts of impervious cover and faster urbanization rates in most
instances. Urbanization is clearly driving the abundance, species richness and behavior of ladybird
beetles in California, as we have found in previous studies [29,50]. However, we show that this
is not the case in another environmental context (Michigan). Though not specifically sampled in
urban gardens, a majority of taxa decline in abundance and species richness with urbanization [2].
This is particularly apparent for vertebrates [18], but is also often the case for invertebrates [51–53].
In contrast, plant species generally increase with urbanization presumably because non-native species
introductions outweigh extinctions in this group and because plants have smaller geographical ranges
than mobile organisms with high dispersal abilities [54]. Organisms with larger ranges may be
more sensitive to urbanization because urbanization can fragment migratory corridors and impede
dispersal [55,56]. Given that we observed divergent geographical responses to urbanization most
strongly for unique ladybird species and one similar response to urbanization by shared species,
differences in dispersal ranges could possibly explain our results. If unique beetles to California have
larger geographical distributions—often related to species dispersal ability and range size [57]—than
beetles unique to Michigan, our results would be consistent with the dispersal hypothesis. However,
we did not find strong evidence for this hypothesis in our results, because the reported geographic
distribution for these species is relatively narrow for California beetles versus Michigan beetles
(Table 1).
It is important to note, however, that though general trends in taxonomic responses to urbanization
exist, all taxa that have been examined at multiple spatial scales or contexts exhibit some degree of
divergence in responses to urbanization (6.9 to 33.3% of studies in a given taxon report different
responses to urbanization depending on context) [2,28,30,58,59]. At larger spatial scales, urbanization
is correlated with dense human populations that also coincide historically with nutrient-rich and
biodiverse regions [60,61]. McKinney suggests that this can produce an apparent positive effect
of urbanization on species abundance and richness [2]. Moreover, the longer periods of warm
temperatures due to urbanization (i.e., urban heat island effects) may increase insect population
abundance because of increased reproductive capacity [62], a common physiological response for
arthropods [63]. At smaller spatial scales, local effects including management intensity and the
destruction of habitat and pollution may impose negative effects of urbanization on species abundance
and richness [64]. However, our results do not support this hypothesis given that ladybird beetles
responded negatively to urbanization at larger spatial scales in Michigan, and positively at smaller
spatial scales in California (Figure 2, Table 1).
The rate of urbanization, not only the amount of impervious surface, was important for explaining
beetle abundance and diversity but exhibited different patterns depending on the group. Interestingly,
while the abundance and diversity of unique species similarly diverged in regional responses to
urbanization rate as to amount of impervious surface, shared species all showed positive unidirectional
responses to urbanization rate. The predictor variables are not significantly correlated, and thus couldSustainability 2018, 10, 1829 11 of 17
theoretically have divergent effects (Table S1). Urbanization rates were actually relatively similar in
California and in Michigan (at 500 m), which could explain why shared species had similar responses
in each region while unique species had opposite responses. The differences in ladybird biodiversity
between regions is therefore likely best explained by a species-level response: specifically, the response
of unique species to California versus Michigan. Indeed, the strongest pattern from our study is the
response of unique species to both the percent impervious surface and to the rate of urbanization,
with abundance of unique beetles significantly increasing in California but decreasing in Michigan.
This suggests that there are environmental filters at regional as well as local scales for species’ traits
that allow them to thrive in more urban areas and habitats [12,65] in California, and that in Michigan,
those species are not present. Only species with traits that allow them to persist in urban environments
should similarly increase with increasing rates of urbanization across regions. Indeed, traits including
habitat, diet breadth and foraging efficiency have explained the global expansion of the ladybird
species Harmonia axyridis into urban areas [66,67]. The similar unidirectional response of shared species
to urbanization rate in our study supports this hypothesis.
Thus, our results may be explained by the legacy of land use change in each region and species’
life histories/traits. California gardens have more species and more unique species that are not found
in Michigan. Michigan gardens have fewer species, and 50% of those species were also found in
California gardens. Most of the shared species across regions are aphidophagous (eat aphids), while in
California the unique species to the region largely eat mites, scales and fungus (Table 1). For example,
the fungus feeder Psyllobora vigintimaculata is very abundant in California and has a different life
history than other species (Figure S2). The presence of species with these feeding preferences could be
because of the industrial agricultural crops grown within and near our urban garden sites in California,
historically and currently. Some of the region was once an orchard landscape, known as the “Valley of
Heart’s Delight”, that has historically grown diverse fruit and nut trees [68]. Fruit trees and landscaped
shrubs are often prone to scale, mite and mealybug pest damage along with crops like strawberries
and tomatoes [69]. As discussed earlier, human populations preferentially settle in biodiverse areas (or
“biodiversity hotspots”) [61,70], and cities can coincide with threatened species distribution [71,72],
possibly explaining positive relationships between ladybirds and urbanity. The legacy of agriculture in
turn has permanent effects on ecosystems, and the influx of nutrients and irrigation can also create
biodiversity hotspots [60]. Natural enemies were historically introduced from e.g., New Zealand
and Australia for biological control of pests in the orchards. For example, the Dusky ladybird beetle,
Nephus binaevatus, was released into California from New Zealand in 1922 to help control mealybugs in
orchards [73]. This non-native species is unique to the California garden sites, particularly in very urban
sites in Santa Clara county that were once orchards. Our sampled garden sites in California contain
fruit trees such as citrus and stone fruit. Thus, some of the unique ladybird beetles like N. binaevatus
and also Coccinella septempuctata are legacies of agricultural industrialization and urbanization unique
to California, and/or may be present in gardens due to the availability of their prey/host.
The ladybird beetles in California—particularly those that are unique—may be more likely able to
withstand environmental disturbance because they have been historically used in human-dominated
systems for e.g., biological control. Non-native species to a region often have a greater ability to survive in a
variety of habitats—including disturbed habitats—than native species [74]. In disturbed urban landscapes,
more abundant species are habitat generalists and/or non-native to a region [2,75]. These species have
ecological traits that allow them to exploit resources and persist [76], and environmental filters have
been used to explain taxonomic differences between urban habitats [12,77]. Most (though not all) of
the ladybird species that we observed in Michigan sites are native species from the greater Northeast
and Midwest region (Table 1). This could explain why abundance and richness of beetles declines with
urbanization in Michigan: many of the species are native and are less likely to survive and adapt to
environmental disturbances like urbanization as non-native and invasive species [78].
Abiotic factors associated with urbanization and different environmental contexts may better
explain the contrasts in ladybird diversity patterns in California and Michigan agroecosystems.Sustainability 2018, 10, 1829 12 of 17 Ladybirds must avidly consume water (e.g., dew, rain) for their survival [79], and water availability often drives their movement ecology and life cycle [80]. Thus, climate patterns (temperature, precipitation) can affect ladybird distribution [39,79], and significant climatic contrasts between regions could explain divergent patterns in ladybird abundance and species richness in gardens. In comparison to Michigan, which has a temperate climate with four defined seasons, California has on average warmer temperatures throughout the year and two seasons, one dry (summer; April to September) and one wet (winter; October to March). In California, urban gardens in the summer dry months (with
Sustainability 2018, 10, 1829 13 of 17
Supplementary Materials: The following are available online at http://www.mdpi.com/2071-1050/10/6/1829/s1,
Figure S1: Species accumulation curves, Figure S2: Histograms of ladybird species sampled, Table S1: Correlations
between explanatory variables, Table S2: Ladybird beetle sensitivity to percent impervious surface at various
spatial scales.
Author Contributions: All authors conceived of and designed the study and performed the data collection; T.W.O.
and K.L. analyzed the data; M.H.E. drafted the manuscript. All authors provided feedback on and contributed
significantly to the manuscript.
Acknowledgments: We thank the field and lab work provided by P. Bichier, Y. Bravo, J. Burks, H. Cohen,
V. De la Fuente, K. Ennis, A. García, P. Gillette, M. Hash, R. Hruska, B. Ferguson, M. MacDonald, L. Marin,
H. Morales, M.E. Narvaez Cuellar, M. Otoshi, M. Plascencia, R. Quistberg, G. Santiz Ruiz, R. Schreiber-Brown,
S-S. Thomas, L. Hawkes, B. Madden, A. Ho and D. Kowalsky. We thank the two anonymous reviewers for their
helpful comments on the manuscript. Thank you to S. Philpott, J. Vandermeer, and I. Perfecto for considerable
research support. We thank the community gardens and gardeners for hosting our research in California: Aptos
Community Garden, Beach Flats Community Garden, Berryessa Community Garden, the Center for Agroecology
and Sustainable Food Systems, Chinatown Community Garden, Coyote Creek Community Garden, El Jardín at
Emma Prusch Park, The Forge at Santa Clara University, Giving Garden at Faith Lutheran Church, Homeless
Garden Project, La Colina Community Garden, Laguna Seca Community Garden, Live Oak Green Grange
Community Garden, MEarth at Carmel Valley Middle School, Mi Jardín Verde Community Garden at All Saints’
Episcopal Church, Our Green Thumb Garden at Middlebury Institute of International Studies, and Salinas
Community Garden at St. George’s Episcopal Church. We thank Project Grow Community Gardens for hosting
our research in Michigan. This research was financially supported by the Center for Agroecology and Sustainable
Food Systems and the Environmental Studies Department at the University of California, Santa Cruz. M.H.E. was
supported by a National Science Foundation Graduate Research Fellowship Grant No. 174835. T.W.O was funded
by the Department of Ecology and Evolutionary Biology and the Rackham Graduate School at the University
of Michigan. This material is based upon work supported by the National Science Foundation under Grant
No. 1711167 to T.W.O.
Conflicts of Interest: The authors declare no conflict of interest. The founding sponsors had no role in the design
of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the
decision to publish the results. The data was collected with site approval.
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